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Title: Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform

Abstract

The feasibility of heterotrophic-phototrophic symbioses was tested via pairing of yeast strains Cryptococcus curvatus, Rhodotorula glutinis, or Saccharomyces cerevisiae with a sucrose-secreting cyanobacterium Synechococcus elongatus. The phototroph S. elongatus showed no growth in standard BG-11 medium with yeast extract, but grew well in BG-11 medium alone or supplemented with yeast nitrogen base without amino acids (YNB w/o aa). Among three yeast species, C. curvatus and R. glutinis adapted well to the BG-11 medium supplemented with YNB w/o aa, sucrose, and various concentrations of NaCl needed to maintain sucrose secretion from S. elongatus, while growth of S. cerevisiae was highly dependent on sucrose levels. R. glutinis and C. curvatus grew efficiently and utilized sucrose produced by the partner in co-culture. Co-cultures of S. elongatus and R. glutinis were sustained over 1 month in both batch and in semi-continuous culture, with the final biomass and overall lipid yields in the batch co-culture 40 to 60% higher compared to batch mono-cultures of S. elongatus. The co-cultures showed enhanced levels of palmitoleic and linoleic acids. Furthermore, cyanobacterial growth in co-culture with R. glutinis was significantly superior to axenic growth, as S. elongatus was unable to grow in the absence of the yeast partner whenmore » cultivated at lower densities in liquid medium. Accumulated reactive oxygen species was observed to severely inhibit axenic growth of cyanobacteria, which was efficiently alleviated through catalase supply and even more effectively with co-cultures of R. glutinis. In conclusion, the pairing of a cyanobacterium and eukaryotic heterotroph in the artificial lichen of this study demonstrates the importance of mutual interactions between phototrophs and heterotrophs, e.g., phototrophs provide a carbon source to heterotrophs, and heterotrophs assist phototrophic growth and survival by removing/eliminating oxidative stress. Our results establish a potential stable production platform that combines the metabolic capability of photoautotrophs to capture inorganic carbon with the channeling of the resulting organic carbon directly to a robust heterotroph partner for producing biofuel and other chemical precursors.« less

Authors:
 [1];  [1];  [2];  [3];  [4];  [1];  [1]
  1. Johns Hopkins Univ., Baltimore, MD (United States). Department of Chemical and Biomolecular Engineering
  2. Johns Hopkins Univ., Baltimore, MD (United States). Department of Biophysics
  3. Harvard Medical School (HMS), Boston, MA (United States). Dept. of Systems Biology; Harvard Univ., Boston, MA (United States). Wyss Inst. for Biologically Inspired Engineering
  4. National Renewable Energy Lab. (NREL), Golden, CO (United States). National Bioenergy Center
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States); Johns Hopkins Univ., Baltimore, MD (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE)
OSTI Identifier:
1351861
Alternate Identifier(s):
OSTI ID: 1485587
Report Number(s):
NREL/JA-5100-68306
Journal ID: ISSN 1754-6834
Grant/Contract Number:  
SC0012658; AC36-08GO28308
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; cyanobacteria; yeasts; co-culture; sucrose; ROS; artificial lichen; hydrogen peroxide; lipid production; Co‑culture; Artifcial lichen

Citation Formats

Li, Tingting, Li, Chien-Ting, Butler, Kirk, Hays, Stephanie G., Guarnieri, Michael T., Oyler, George A., and Betenbaugh, Michael J. Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform. United States: N. p., 2017. Web. doi:10.1186/s13068-017-0736-x.
Li, Tingting, Li, Chien-Ting, Butler, Kirk, Hays, Stephanie G., Guarnieri, Michael T., Oyler, George A., & Betenbaugh, Michael J. Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform. United States. doi:10.1186/s13068-017-0736-x.
Li, Tingting, Li, Chien-Ting, Butler, Kirk, Hays, Stephanie G., Guarnieri, Michael T., Oyler, George A., and Betenbaugh, Michael J. Tue . "Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform". United States. doi:10.1186/s13068-017-0736-x. https://www.osti.gov/servlets/purl/1351861.
@article{osti_1351861,
title = {Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform},
author = {Li, Tingting and Li, Chien-Ting and Butler, Kirk and Hays, Stephanie G. and Guarnieri, Michael T. and Oyler, George A. and Betenbaugh, Michael J.},
abstractNote = {The feasibility of heterotrophic-phototrophic symbioses was tested via pairing of yeast strains Cryptococcus curvatus, Rhodotorula glutinis, or Saccharomyces cerevisiae with a sucrose-secreting cyanobacterium Synechococcus elongatus. The phototroph S. elongatus showed no growth in standard BG-11 medium with yeast extract, but grew well in BG-11 medium alone or supplemented with yeast nitrogen base without amino acids (YNB w/o aa). Among three yeast species, C. curvatus and R. glutinis adapted well to the BG-11 medium supplemented with YNB w/o aa, sucrose, and various concentrations of NaCl needed to maintain sucrose secretion from S. elongatus, while growth of S. cerevisiae was highly dependent on sucrose levels. R. glutinis and C. curvatus grew efficiently and utilized sucrose produced by the partner in co-culture. Co-cultures of S. elongatus and R. glutinis were sustained over 1 month in both batch and in semi-continuous culture, with the final biomass and overall lipid yields in the batch co-culture 40 to 60% higher compared to batch mono-cultures of S. elongatus. The co-cultures showed enhanced levels of palmitoleic and linoleic acids. Furthermore, cyanobacterial growth in co-culture with R. glutinis was significantly superior to axenic growth, as S. elongatus was unable to grow in the absence of the yeast partner when cultivated at lower densities in liquid medium. Accumulated reactive oxygen species was observed to severely inhibit axenic growth of cyanobacteria, which was efficiently alleviated through catalase supply and even more effectively with co-cultures of R. glutinis. In conclusion, the pairing of a cyanobacterium and eukaryotic heterotroph in the artificial lichen of this study demonstrates the importance of mutual interactions between phototrophs and heterotrophs, e.g., phototrophs provide a carbon source to heterotrophs, and heterotrophs assist phototrophic growth and survival by removing/eliminating oxidative stress. Our results establish a potential stable production platform that combines the metabolic capability of photoautotrophs to capture inorganic carbon with the channeling of the resulting organic carbon directly to a robust heterotroph partner for producing biofuel and other chemical precursors.},
doi = {10.1186/s13068-017-0736-x},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 10,
place = {United States},
year = {2017},
month = {3}
}

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Figures / Tables:

Fig. 1 Fig. 1: Axenic growth of different yeast strains. a–c Effect of medium components on monoculture of yeasts; “BG” indicates BG-11 added with 2 g/L sucrose, 4 mM ammonium chloride, 1 mM IPTG, and 100 mM NaCl; “BG + YNB w/o aa” indicates “BG” supplied with YNB w/o aa; “BG +more » YE” indicates “BG” supplied with YE. d–f Effect of glucose/sucrose and light/dark on monoculture of yeasts; Medium used here was BG-11[co] supplied with 2 g/L sucrose or 2 g/L glucose, as indicated in the legends. g–i Effect of sucrose concentration on monoculture of yeasts; Medium used here was BG-11[co] supplied with various concentration of sucrose, as indicated in the legends. j–l Effect of NaCl concentration on monoculture of yeasts. Medium here was BG-11[co] supplied with 2 g/L sucrose, but with adjusted NaCl concentration in each condition. a, d, g, j for C. curvatus; b, e, h, k for R. glutinis; c, f, i, l for S. cerevisiae. Light condition was used if no specific statement. All data are averages of biological triplicates ± standard deviation« less

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    Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.